Locomotor systems are a particularly rich arena in which to pursue studies of dynamic, evolving relationships between structure and function: animals move through their environments in a myriad of ways that are of central importance to all aspects of their natural history. These patterns of motion depend directly on intricate, multi-faceted systems of organs and tissues that are amenable to structural and mechanical analyses. Locomotion is at once of direct relevance to many arenas of study — ecology, evolution, physiology, mechanics, materials science, neuroscience, genetics and more — and can therefore provide an ideal context in which to explore questions concerning morphological design and evolution.
I began my career with a primary focus on the locomotor systems of hominoid primates, particularly brachiation in gibbons, and my work with this highly pendulum-like form of locomotion helped shape my interest in applying the physical science approaches of mechanics and energetics to organisms. Since then, I have remained interested in terrestrial locomotion in primates and other mammals, but have invested the greater part of my effort toward the study of flight in bats, in questions regarding size and scale and the structural architecture of locomotor systems; and in the mechanics of the cuticular exoskeleton of insects.
Structure and Motion of Bat Wings
Until recently, biologists have viewed vertebrate wings in general, and bat wings in particular, as analogs of the fixed wings of human-engineered vehicles: stationary, rigid airfoils similar to those of fixed-wing aircraft. However, at the Reynolds numbers at which bats fly, between 103 and 106, the effects of viscosity are not negligible, as they are for even small airplanes. In this Re range, flow over foils can be turbulent, unsteady, and unpredictable, and basic parameters such as wing aspect ratio, angle of attack, camber, etc., can influence flow patterns and aerodynamic forces in dramatically different ways than in higher Re flows. Our lab has adopted an approach that integrates biological and physical studies of natural and naturalistic flight in diverse living bats, physical experiments employing models that mimic key features of the bat flight apparatus, and computational simulation of aspects of bat flight.
We have developed and implemented methods to document the complex motions of wings of a diversity of bats in flight, and have shown that complex, dynamically changing 3D wing topology is the rule in even ‘simple’ constant speed, level flight of bats. These patterns remain consistent over a large range of body sizes, but show variations among bats from widely separated lineages. Bats employ even more dynamically complex and subtle motions in carrying out turning motions and more sophisticated maneuvers.
In parallel with studies of wing motion, we have probed the variation in material properties of the mechanically important tissues of the bat wing. We have shown that the mineral content declines substantially from the shoulder to the wingtip, with variation in mineralization in a single bat often more than encompassing the entire previously documented range of variation for all mammalian limb bones. Similarly, the skin of a single wing encompasses an extraordinary range of mechanical characteristics in direct relation to the underlying gross architecture of the wing’s collagen-elastin structural network, and differs both among wing regions and among taxa, with large-bodied, load-carrying taxa characterized by some of the strongest and stiffest skin tissue found among mammals. In keeping with energetic constraints on flight, bat skin is several times thinner than predictions based on body size, and thus meets unusually extreme mechanical demands with a significantly reduced mass.
Experimental Fluid Dynamics
We carry out wind tunnel studies of bat flight wakes coupled with detailed kinematics at high temporal and spatial resolution. We have found that the distinct patterns of wing movements employed by bats generate characteristic wakes that differ from those of birds and insects. Moreover, we find that wake structure can differ substantially among bat species, almost as much as between wakes of a bird and a bat of comparable body size.
Our experimental efforts also encompass physical models that capture important aspects of the bat flight apparatus in somewhat simplified, abstracted form. For example, unlike birds and insects, bats and the lineages of mammals that specialize in gliding locomotion employ airfoils made of compliant material, a fact few aerodynamicists recognized until our work. We have carried out experimental studies of compliant airfoils demonstrating their remarkable capacity to generate lift at zero and very high angles of attack, and have documented the physical bases of this phenomenon; compliant airfoils can be self-cambering in even minimal flows, and interact with flows in a manner that facilitates persistence of attached flow in conditions that would cause stall for rigid airfoils. Our most sophisticated and complex physical models are bat-like robots that capture many aspects of realistic bat flight with high fidelity, and allow us to study force production and flow dynamics. Because these experiments allow us to independently modulate characteristics of the “flyer” in a manner that is impossible in living animals, we are able to tease apart the roles of motion and materials on aerodynamics and energetics in a way that is impossible working with living animals alone.
Three years ago, my colleague and friend Tom Kunz paid a visit to me from Boston University. He sat in my office, looked directly at me and announced, grinning, “There are fields called terrestrial ecology and marine ecology. It’s time to have Aeroecology.” I laughed, not quite realizing the seriousness under the smile. Tom challenged me to help him define what the explicit recognition of such a discipline might mean to those who study animal flight; in doing so, I find my thinking about interesting and important research questions changing in subtle ways. In an aeroecological perspective, we recognize that the physical environment of the aerosphere is both complex and dynamic, and poses many challenges to the locomotor systems of the three extant evolutionary lineages of flying animals. Many features of the aerosphere, operating over spatial and temporal scales of many orders of magnitude, have the potential to be important influences on animal flight.
Much as marine ecologists have studied the relationship between physical oceanography and swimming locomotion, a subfield of aeroecology can focus attention on the ways the biology of flight is influenced by these characteristics. Airflows are altered and modulated by motion over and around natural and human-engineered structures, and vortical flow structures, turbulence, etc., are introduced to the aerial environment by technologies such as aircraft and wind farms. Diverse aspects of the biology of flight may be better understood with reference to an aeroecological approach, particularly the mechanics of flight, flight energetics, the sensing of aerial flows, and the motor control of flight. To date, I have begun to collect data concerning the natural flight behaviors of bats exiting large cave colonies for evening foraging bouts along with quantifying ambient flow conditions at the time and location of fly-out. In the long run, I hope to be able to link observations of natural flight behaviors to the more carefully controlled studies of flight mechanics and energetics we carry out in the lab. Flight biologists can offer considerable insight into the ecology of the aerial world, and an aeroecological approach holds great promise for stimulating and enriching the study of flight biology.